Autophagy of the somatic stalk cells likely nurses the propagating spores of Dictyostelid social amoebas [version 2; peer review: 1 approved, 2 approved with reservations]

Qingyou Du, Pauline Schaap (Lead / Corresponding author)

Research output: Contribution to journalArticlepeer-review

19 Downloads (Pure)

Abstract

Background: Autophagy (self-feeding) assists survival of starving cells by partial self-digestion, while dormancy as cysts, spores or seeds enables long-term survival. Starving Dictyostelium amoebas construct multicellular fruiting bodies with spores and stalk cells, with many Dictyostelia still able to encyst individually like their single-celled ancestors. While autophagy mostly occurs in the somatic stalk cells, autophagy gene knock-outs in Dictyostelium discoideum ( D. discoideum) formed no spores and lacked cAMP induction of prespore gene expression. Methods: To investigate whether autophagy also prevents encystation, we knocked-out autophagy genes atg5 and atg7 in the dictyostelid Polysphondylium pallidum, which forms both spores and cysts. We measured spore and cyst differentiation and viability in the knock-out as well as stalk and spore gene expression and its regulation by cAMP. We tested a hypothesis that spores require materials derived from autophagy in stalk cells. Sporulation requires secreted cAMP acting on receptors and intracellular cAMP acting on PKA. We compared the morphology and viability of spores developed in fruiting bodies with spores induced from single cells by stimulation with cAMP and 8Br-cAMP, a membrane-permeant PKA agonist. Results: Loss of autophagy in P. pallidum reduced but did not prevent encystation. However, spore, but not stalk differentiation, and cAMP-induced prespore gene expression were lost. Spores induced in vitro by cAMP and 8Br-cAMP were smaller and rounder than spores formed multicellularly and while they were not lysed by detergent they did not germinate, unlike multicellular spores. Conclusions: The stringent requirement of sporulation on both multicellularity and autophagy, which occurs mostly in stalk cells, suggests that stalk cells nurse the spores through autophagy. This highlights autophagy as a major cause for somatic cell evolution in early multicellularity.

Original languageEnglish
Article number104
Number of pages33
JournalOpen Research Europe
Volume2
Early online date23 Sep 2022
DOIs
Publication statusPublished - 23 Nov 2022

Keywords

  • Autophagy
  • Dictyostelia
  • Encystation
  • Evolution of multicellularity
  • Evolution of soma
  • Sporulation

Fingerprint

Dive into the research topics of 'Autophagy of the somatic stalk cells likely nurses the propagating spores of Dictyostelid social amoebas [version 2; peer review: 1 approved, 2 approved with reservations]'. Together they form a unique fingerprint.

Cite this